Department of Primatology

Current Projects

Social relationships and stress

Adult female Rafiki (left) had an unusually close relationship with the alpha male, Fonz. Here they are engaging in the vulnerable contact behavior dubbed ‘handsniffing’.

Whether due to variation in early life experience or genetic diversity, individuals within a species can exhibit a wide-range of social styles and abilities to cope with stress. Besides inevitable physiological and environmental stressors, such as fluctuations in weather, food shortages, and pregnancy; capuchins create social stress worthy of a soap opera. Female capuchins stay in the group with their female relatives for the entirety of their long lives, and thus have both opportunity and the need to build strong relationships. Reliable allies are important, as capuchins exhibit a high frequency of cooperation and coalition and engage in lethal aggression. In a coalition, females can outrank a male. Together, they can defend the group against outsiders, who might otherwise prevent access to valuable territory or takeover the group and kill infants.

Yet capuchin females, like humans, vary greatly in how they invest in social relationships. One might attempt to gain favor by grooming everyone she can, while another avoids the group except for rare play bouts with a single friend. Much of female-female interaction is in the form of grooming, but some of the monkeys at Lomas Barbudal also engage in peculiar vulnerable contact behaviors. These learnt interactions are unique to each pair that practices them, but generally involve a dangerous combination of body parts: the fingers of one partner in the nose and eyes of the other, one’s tail in the other’s mouth, chunks of hair torn slowly off the face and then traded back and forth. These seemly uncomfortable exchanges are performed with a slow, almost trance-like attitude. Despite observing them for more than twenty years, researchers are still intrigued by the question of what function these behaviors might serve. Zahavi (1977) hypothesized that uncomfortable or risky interactions could serve to test bonds within a dyad because individuals who are committed to maintaining such an interaction are likely to be dedicated to the relationship and cooperate in the future. Maintenance of the interaction could prepare participants for future coordinated actions and reinforce the social support between them (Perry et al., 2003). As a pair develops their particular routine, they could become comfortable with this intimate contact and the signal of a trusting relationship could function as a buffer or relief from stress. A hug can function in much the same way for humans; a stranger wrapping his arms around you and squeezing could be terrifying, but the same gesture from a friend can turn around a bad day.

My primary question is how social style, and particularly engaging in vulnerable contact behaviors, influences how individuals cope with stress. Is it better to have a large quantity of allies, or just a few high-quality relationships? Are vulnerable contact behaviors a particularly salient signal of relationship quality? I am examining responses to acute stressful events by measuring fecal glucocorticoids from females that I followed continuously for sufficient time to connect the event with the appearance of the respective hormones in feces. This is a relatively new approach in the field, as researchers typically collect samples opportunistically or after following an individual for a short interval (10 minutes – 1 hour). Without following the subject for the entire time it takes for hormones entering the bloodstream to arrive in the intestines and be excreted, one cannot know the specific events that contribute to the glucocorticoid levels in each fecal sample. In such cases, one can only average the levels of several samples and examine stress levels as a ‘chronic’ condition. The challenge of studying responses to acute stressors can not only inform my own research questions, but also help refine the methods of field endocrinology.

I owe the possibility and opportunity of conducting this study to Dr. Susan Perry, who, through years of perseverance and passion, established a long-term research site with enough detailed data on the monkeys. Without the most tireless and dedicated field assistants in the world, my methods would have been a pipedream. I am grateful to Dr. Patricia Whitten for supporting my ideas and allowing me to work in her Laboratory of Reproductive Ecology and Environmental Toxicology at Emory University. This project was funded by The National Science Foundation, The Leakey Foundation, and the Hartley Corporation/SDE fellowship from Graduate Women in Science.

Stress responses to the risk of infanticide

Caption: 5-month old male, Bedlam, seems both excited and anxious to be riding the back of Oden, the alpha male, who is not his father.

In many species, a male must defeat others to obtain breeding opportunities. This success is often short-lived. New, younger and stronger males will soon challenge him for his position. If the time between births of new infants to a mother is longer than a male’s likely tenure, he can increase his reproductive success by killing the un-weaned infants of his potential mates, thus speeding their return to a fertile state (the sexual selection hypothesis, Hrdy, 1974). Although we have observed some extraordinarily long alpha-male tenures at Lomas Barbudal (18 years!), the average tenure length is under one year, while the average inter-birth-interval is 28 months. Accordingly, infant survival in the year after an alpha-male turnover drops precipitously to only 18% compared to 88% in stable years (Fedigan, 2003). Infanticide is the primary cause of death in the first year of life. Given the huge investment of capuchin females in each of their offspring, a change in the alpha male, and subsequently, the intentions of the new alpha male, should be a primary source of stress. But, only for females who are pregnant or nursing an infant fathered by a previous alpha male. Young females ready for their first pregnancy and mothers whose infants can already survive without nursing should embrace the new alpha male and begin forging a good relationship with him. We don’t know if capuchin mothers really follow these strategies, or if they are aware of their situation, especially when the threat is less tangible (e.g. the risk to an unborn infant when an alpha-turnover occurs during the pregnancy).

Fecal glucocorticoids can be a window into how females experience changes in the male hierarchy. By measuring the stress hormones from females in different reproductive states during periods of peace, instability, and everything in between, we aim to address such questions as whether females whose infants are at risk are more stressed than cycling females by an alpha turnover, and whether this response varies according to whether the new alpha is familiar or related to the previous alpha. Capuchin mothers often have little helpers – juveniles who ‘allomother’ by keeping an eye on and carrying the infant. We are also interested in whether allomothers are stressed by a threat of infanticide to their infant charges. By comparing fecal glucocorticoids of juveniles that care for an infant at risk to those of juveniles who aren’t allomothers or who are allomothers to infants not at risk, we hope to enhance the picture of how broadly the risk of infanticide affects capuchin society.

This project would not be possible without the collaborative efforts of a multitude of people. Samples and demographic information for this project have been collected by many dedicated assistants of Susan Perry’s Lomas Barbudal Capuchin Project over the years. Sample analysis is performed at the MPI-EVA endocrinology lab with the guidance of Dr. Tobias Deschner and the laboratory skills of Franka Simea Schaebs. Also essential to this project are my stipend support from the German Academic Exchange, the use of facilities and institutional support provided by the Max Planck Society, and a COR grant to Dr. Perry for laboratory expenses.

Habitat destruction and stress

Human activity has both direct and indirect impacts on the lives of other organisms. Not all consequences of human activity are obvious, as the effects may be separated in time and space from the original action. Moreover, physiological effects on organisms may not be apparent by simple observation or occasional censusing, yet can have long-term effects on health and reproductive success. Capuchin monkeys are a generalist species, capable of living in a great variety of habitats, with a very broad omnivorous diet, and the potential to reproduce year-round. Such a highly adaptable species provides a good model to examine the hidden physiological effects of human activity because individuals are able to survive, at some cost, despite non-ideal conditions. More specialized species often disappear altogether from forests with substantial human disturbance, leaving the cause difficult to determine. Thus, capuchin responses to human activities can also serve as a conservative estimate of the physiological response of more sensitive species.

The monkeys of the Lomas Barbudal Monkey Project do not restrict themselves to the boundaries of biological reserve. The tropical dry forest in which they live is considered the most threatened forest-type in the world, and centuries of cattle ranging have left only islands of habitat suitable for capuchins. Still, forests with various levels of protection border the reserve, and some of our research groups manage to live entirely within these threatened areas. One of these groups has experienced massive habitat destruction that not only took away the core of their territory, but also interferes with their access to fresh water. I am investigating whether these individuals were chronically stressed by these conditions by comparing their fecal glucorticoids in two ways: testing for changes over time, and relative to another group from which they split prior to the major destruction.

The monkeys of one study group must climb down a cliff, cut into the forest as part of the expansion of a quarry, and cross a road in to order to reach the river that is sometimes the only source of fresh water in the dry season.